Nanomedicine for the eradication of Helicobacter pylori: recent advances, challenges and future perspective

References

• Li Y , ChoiH , LeungK , JiangF , GrahamDY , LeungWK. Global prevalence of H. pylori infection between 1980 and 2022: a systematic review and meta-analysis. Lancet Gastroenterol. Hepatol.8(6), 553–64 (2023).
   PubMed Web of Science ®Google Scholar
• Gu SX , SiddonAJ , HuntingtonSF , JainD. H. pylori–negative mucosa-associated lymphoid tissue [MALT] lymphoma of the stomach: a clinicopathologic analysis. Am. J. Clin. Pathol.160(6), 612–619 (2023).
   PubMed Web of Science ®Google Scholar
• Gholamhosseinzadeh E , GhalehnoeiH , KazemiVeisari A , SheidaeiS , GoliHR. Frequency of significant virulence genes in gastric biopsies of H. pylori-positive patients with gastritis. AMB Express13(1), 1–8 (2023).
   PubMed Web of Science ®Google Scholar
• Chin A , TayY , MarshallBJ. H. pylori interpretation in 2022. Gut Microbiota Integrat. Wellness.1, 2023 (2023).
   Google Scholar
• Morsy T , Abou-ElmagdA , MousaA. Zoonotic Giardiasis and its complications: a review article. J. Egypt. Soc. Parasitol.53(2), 387–400 (2023).
   Google Scholar
• Hanyu H , EngevikKA , MatthisAL , OttemannKM , MontroseMH , AiharaE. H. pylori uses the TlpB receptor to sense sites of gastric injury. Infect. Immun.87(9), e00202–e00219 (2019).
   PubMed Web of Science ®Google Scholar
• Idowu S , BertrandPP , WalduckAK. Gastric organoids: advancing the study of H. pylori pathogenesis and inflammation. Helicobacter27(3), e12891 (2022).
   PubMed Web of Science ®Google Scholar
• Celli JP , TurnerBS , AfdhalNHet al. H. pylori moves through mucus by reducing mucin viscoelasticity. Proc. Natl Acad. Sci. USA106(34), 14321–6 (2009).
   PubMed Web of Science ®Google Scholar
• Ferreira RM , MachadoJC , LetleyDet al. A novel method for genotyping the H. pylori vacA intermediate region directly in gastric biopsy specimens. J. Clin. Microbiol.50(12), 3983–9 (2012).
   PubMed Web of Science ®Google Scholar
• Arunima A , van SchaikEJ , SamuelJE. The emerging roles of long non-coding RNA in host immune response and intracellular bacterial infections. Front. Infect. Microbiol.13, 1160198 (2023).
   PubMed Web of Science ®Google Scholar
• Sowaid IY , AliOMK , HussianSAS. Extra-gastroduodenal manifestation and H. pylori infection. Arch. Razi Institute77(3), 1017–26 (2022).
   PubMedGoogle Scholar
• Mărginean CD , MărgineanCO , MeliţLE. Helicobacterpylori-related extraintestinal manifestations – myth or reality. Children [Basel, Switzerland]9(9), 1352 (2022).
   PubMed Web of Science ®Google Scholar
• Tseng DS , LiD , CholletiSM , WeiJC , JodestyY , PhamHV. Effect of H. pylori treatment on unexplained iron deficiency anemia. Permanente J.23(3), 1-195 (2019).
   Google Scholar
• Liu WZ , XieY , LuHet al. Fifth Chinese national consensus report on the management of H. pylori infection. Helicobacter23(2), e12475 (2018).
   PubMed Web of Science ®Google Scholar
• Guevara B , CogdillAG. H. pylori: a review of current diagnostic and management strategies. Dig. Dis. Sci.65(7), 1917–31 (2020).
   PubMed Web of Science ®Google Scholar
• Shah SC , IyerPG , MossSF. AGA clinical practice update on the management of refractory H. pylori infection: expert review. Gastroenterology160(5), 1831–41 (2021).
   PubMed Web of Science ®Google Scholar
• Zagari RM , FrazzoniL , MarascoG , FuccioL , BazzoliF. Treatment of H. pylori infection: a clinical practice update. Minerva Med.112(2), 281–7 (2021).
   PubMed Web of Science ®Google Scholar
• Fallone CA , ChibaN , van ZantenSVet al. The Toronto consensus for the treatment of H. pylori infection in adults. Gastroenterology151(1), 51–69.e14 (2016).
   PubMed Web of Science ®Google Scholar
• Malfertheiner P , MegraudF , RokkasTet al. Management of H. pylori infection: the Maastricht VI/Florence consensus report. Gut71(9), 1724–62 (2022).
   Web of Science ®Google Scholar
• Yang H , GuanL , HuB. Detection and treatment of H. pylori: problems and advances. Gastroenterol. Res. Pract.2022:4710964 (2022).
   PubMed Web of Science ®Google Scholar
• Tshibangu-Kabamba E , YamaokaY. H. pylori infection and antibiotic resistance – from biology to clinical implications. Nature rev. Gastroenterol. Hepatol.18(9), 613–29 (2021).
   PubMed Web of Science ®Google Scholar
• Hathroubi S , ZerebinskiJ , ClarkeA , OttemannKM. H. pylori biofilm confers antibiotic tolerance in part via a protein-dependent mechanism. Antibiotics [Basel, Switzerland]9(6), 1–11 (2020).
   Web of Science ®Google Scholar
• Kadkhodaei S , SiavoshiF , AkbariNoghabi K. Mucoid and coccoid H. pylori with fast growth and antibiotic resistance. Helicobacter25(2), e12678 (2020).
   PubMed Web of Science ®Google Scholar
• Rubey KM , BrennerJS. Nanomedicine to fight infectious disease. Adv. Drug Deliv. Rev.179, 113996 (2021).
   PubMed Web of Science ®Google Scholar
• Jackman JA , LeeJ , ChoNJ. Nanomedicine for infectious disease applications: innovation towards broad-spectrum treatment of viral infections. Small.12(9), 1133–9 (2016).
   PubMed Web of Science ®Google Scholar
• Li X , ChenL , LuanSet al. The development and progress of nanomedicine for esophageal cancer diagnosis and treatment. Semin. Cancer Biol.86, 873–85 (2022).
   PubMed Web of Science ®Google Scholar
• Fornaguera C , García-CelmaM. Personalized nanomedicine: a revolution at the nanoscale. J. Pers. Med.7(4), 12 (2017).
   PubMed Web of Science ®Google Scholar
• Hejmady S , PradhanR , AlexanderAet al. Recent advances in targeted nanomedicine as promising antitumor therapeutics. Drug Discov. Today25(12), 2227–44 (2020).
   PubMed Web of Science ®Google Scholar
• Koo OM , RubinsteinI , OnyukselH. Camptothecin in sterically stabilized phospholipid micelles: A novel nanomedicine. Nanomed.: Nanotechnol. Biol. Med.1(1), 77–84 (2005).
   PubMed Web of Science ®Google Scholar
• Couvreur P . Nanoparticles in drug delivery: past, present and future. Adv. Drug Deliv. Rev.65(1), 21–3 (2013).
   PubMed Web of Science ®Google Scholar
• Farokhzad O , LangerR. Nanomedicine: developing smarter therapeutic and diagnostic modalities☆. Adv. Drug Deliv. Rev.58(14), 1456–9 (2006).
   PubMed Web of Science ®Google Scholar
• Lok CN , ZouT , ZhangJJ , LinIWS , CheCM. Controlled-release systems for metal-based nanomedicine: encapsulated/self-assembled nanoparticles of anticancer gold[III]/platinum[II] complexes and antimicrobial silver nanoparticles. Adv. Mater.26(31), 5550–7 (2014).
   PubMed Web of Science ®Google Scholar
• Kim DK , DobsonJ. Nanomedicine for targeted drug delivery. J. Mater. Chem.19(35), 6294 (2009).
   Web of Science ®Google Scholar
• Sandhiya S , DkharSA , SurendiranA. Emerging trends of nanomedicine – an overview. Fundament. Clin. Pharmacol23(3), 263–9 (2009).
   PubMed Web of Science ®Google Scholar
• Lopes D , NunesC , MartinsMCL , SarmentoB , ReisS. Eradication of H. pylori: past, present and future. J. Control. Release189, 169–86 (2014).
   PubMed Web of Science ®Google Scholar
• Kroll AV , FangRH , ZhangL. Biointerfacing and applications of cell membrane-coated nanoparticles. Bioconj. Chem.28(1), 23–32 (2017).
   PubMed Web of Science ®Google Scholar
• Mouriño V , CattaliniJP , BoccacciniAR. Metallic ions as therapeutic agents in tissue engineering scaffolds: an overview of their biological applications and strategies for new developments. J. Royal Soc. Interface9(68), 401–19 (2012).
   PubMed Web of Science ®Google Scholar
• Begg SL . The role of metal ions in the virulence and viability of bacterial pathogens. Biochem. Soc. Transact.47(1), 77–87 (2019).
   PubMedGoogle Scholar
• Chandrangsu P , RensingC , HelmannJD. Metal homeostasis and resistance in bacteria. Nature Rev. Microbiol.15(6), 338–50 (2017).
   PubMed Web of Science ®Google Scholar
• White MF , DillinghamMS. Iron–sulphur clusters in nucleic acid processing enzymes. Curr. Opin. Struct. Biol.22(1), 94–100 (2012).
   PubMed Web of Science ®Google Scholar
• Jablonski PE , LuWP , RagsdaleSW , FerryJG. Characterization of the metal centers of the corrinoid/iron-sulfur component of the CO dehydrogenase enzyme complex from Methanosarcina thermophila by EPR spectroscopy and spectroelectrochemistry. J. Biol. Chem.268(1), 325–9 (1993).
   PubMed Web of Science ®Google Scholar
• Vallee BL , AuldDS. Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry29(24), 5647–59 (1990).
   PubMed Web of Science ®Google Scholar
• Huk OL , CatelasI , MwaleF , AntoniouJ , ZukorDJ , PetitA. Induction of apoptosis and necrosis by metal ions in vitro. J. Arthroplasty19(8), 84–7 (2004).
   PubMed Web of Science ®Google Scholar
• Stafford SL , BokilNJ , AchardMESet al. Metal ions in macrophage antimicrobial pathways: emerging roles for zinc and copper. Biosci. Rep.33(4), e00049 (2013).
   PubMedGoogle Scholar
• Djoko KY , OngC , lynnY , WalkerMJ , McEwanAG. The role of copper and zinc toxicity in innate immune defense against bacterial pathogens. J. Biol. Chem.290(31), 18954–61 (2015).
   PubMed Web of Science ®Google Scholar
• Han D , LiuX , WuS. Metal organic framework-based antibacterial agents and their underlying mechanisms. Chem. Soc. Rev.51(16), 7138–69 (2022).
   PubMed Web of Science ®Google Scholar
• Khursheed R , DuaK , VishwasSet al. Biomedical applications of metallic nanoparticles in cancer: current status and future perspectives. Biomed. Pharmacother.150, 112951 (2022).
   PubMed Web of Science ®Google Scholar
• Evans ER , BuggaP , AsthanaV , DrezekR. Metallic nanoparticles for cancer immunotherapy. Mater. Today21(6), 673–85 (2018).
   Web of Science ®Google Scholar
• Sharma A , GoyalAK , RathG. Recent advances in metal nanoparticles in cancer therapy. J. Drug Target.26(8), 617–32 (2018).
   PubMed Web of Science ®Google Scholar
• Ding SZ , MinoharaY , FanXJet al. H. pylori infection induces oxidative stress and programmed cell death in human gastric epithelial cells. Infect. Immun.75(8), 4030–9 (2007).
   PubMed Web of Science ®Google Scholar
• Li Y , ZhangW , NiuJ , ChenY. Mechanism of photogenerated reactive oxygen species and correlation with the antibacterial properties of engineered metal-oxide nanoparticles. ACS Nano.6(6), 5164–73 (2012).
   PubMed Web of Science ®Google Scholar
• Yin X , LaiY , DuY , ZhangT , GaoJ , LiZ. Metal-based nanoparticles: a prospective strategy for H. pylori treatment. Int. J. Nanomed.18, 2413–29 (2023).
   PubMed Web of Science ®Google Scholar
• Yin X , LaiY , DuY , ZhangT , GaoJ , LiZ. Metal-based nanoparticles: a prospective strategy for H. pylori treatment. Int. J. Nanomed.18, 2413–29 (2023).
   PubMed Web of Science ®Google Scholar
• Zhao F , WuXF. The first bismuth self-mediated oxidative carbonylative coupling reaction via BiIII/BiV redox intermediates. J. Catalysis397, 201–4 (2021).
   Web of Science ®Google Scholar
• Wang Z , ZengZ , WangHet al. Bismuth-based metal–organic frameworks and their derivatives: opportunities and challenges. Coordinat. Chem. Rev.439, 213902 (2021).
   Web of Science ®Google Scholar
• Li H , WangR , SunH. Systems approaches for unveiling the mechanism of action of bismuth drugs: new medicinal applications beyond H. pylori infection. Account. Chem. Res.52(1), 216–27 (2019).
   PubMed Web of Science ®Google Scholar
• Ge R , SunX , GuQet al. A proteomic approach for the identification of bismuth-binding proteins in H. pylori. J. Biol. Inorgan. Chem.12(6), 831–42 (2007).
   PubMed Web of Science ®Google Scholar
• Chen Z , ZhouQ , GeR. Inhibition of fumarase by bismuth[III]: implications for the tricarboxylic acid cycle as a potential target of bismuth drugs in H. pylori. BioMetals25(1), 95–102 (2012).
   PubMed Web of Science ®Google Scholar
• Nazari P , Dowlatabadi-BazazR , MofidMRet al. The Antimicrobial effects and metabolomic footprinting of carboxyl-capped bismuth nanoparticles against H. pylori. Appl. Biochem. Biotechnol.172(2), 570–9 (2014).
   PubMed Web of Science ®Google Scholar
• Chen R , ChengG , SoMHet al. Bismuth subcarbonate nanoparticles fabricated by water-in-oil microemulsion-assisted hydrothermal process exhibit anti-H. pylori properties. Mater. Res. Bull.45(5), 654–8 (2010).
   Web of Science ®Google Scholar
• Fan D , GongY , SunL , ZhangY , ZhangJ. Comparative transcriptome analysis to investigate the mechanism of anti-H. pylori activity of zinc. Microb. Pathogen.168, 105611 (2022).
   PubMed Web of Science ®Google Scholar
• Chakraborti S , BhattacharyaS , ChowdhuryR , ChakrabartiP. The molecular basis of inactivation of metronidazole-resistant H. pylori using polyethyleneimine functionalized zinc oxide nanoparticles. PLOS ONE8(8), e70776 (2013).
   PubMed Web of Science ®Google Scholar
• Attia HG , AlbarqiHA , SaidIG , AlqahtaniO , RaeyMAEI. Synergistic effect between amoxicillin and zinc oxide nanoparticles reduced by oak gall extract against H. pylori. Molecules27(14), 4559 (2022).
   PubMed Web of Science ®Google Scholar
• Saravanan M , GopinathV , ChaurasiaMK , SyedA , AmeenF , PurushothamanN. Green synthesis of anisotropic zinc oxide nanoparticles with antibacterial and cytofriendly properties. Microb. Pathogen.115, 57–63 (2018).
   PubMed Web of Science ®Google Scholar
• Jana S , PalT. Synthesis, characterization and catalytic application of silver nanoshell coated functionalized polystyrene beads. J. Nanosci. Nanotechnol.7(6), 2151–2156 (2007).
   PubMed Web of Science ®Google Scholar
• de Camargo BAF , SilvaDES , da SilvaANet al. New silver[I] coordination compound loaded into polymeric nanoparticles as a strategy to improve in vitro anti-H. pylori activity. Mol. Pharmaceut.17(7), 2287–98 (2020).
   PubMed Web of Science ®Google Scholar
• Gurunathan S , JeongJK , HanJW , ZhangXF , ParkJH , KimJH. Multidimensional effects of biologically synthesized silver nanoparticles in H. pylori, Helicobacter felis, and human lung [L132] and lung carcinoma A549 cells. Nanoscale Res. Lett.10(1), 35 (2015).
   PubMedGoogle Scholar
• Grande R , SistoF , PucaVet al. Antimicrobial and antibiofilm activities of new synthesized silver ultra-nanoclusters [SUNCs] against H. pylori. Front. Microbiol.11, 1705 (2020).
   PubMed Web of Science ®Google Scholar
• Graves JL , TajkarimiM , CunninghamQet al. Rapid evolution of silver nanoparticle resistance in Escherichia coli. Front Genet6, 42 (2015).
   PubMed Web of Science ®Google Scholar
• Lv MM , FanSF , WangQL , LvQY , SongX , CuiHF. An enzyme-free electrochemical sandwich DNA assay based on the use of hybridization chain reaction and gold nanoparticles: application to the determination of the DNA of H. pylori. Microchim. Acta187(1), 73 (2020).
   Web of Science ®Google Scholar
• Gill P , AlvandiAH , Abdul-TehraniH , SadeghizadehM. Colorimetric detection of H. pylori DNA using isothermal helicase-dependent amplification and gold nanoparticle probes. Diagn. Microbiol. Infect. Dis.62(2), 119–24 (2008).
   PubMed Web of Science ®Google Scholar
• Kermanshahian K , YadegarA , MoghimiH , GhourchianH. The synergy of Fe3O4@Au and molybdate as HRP-mimetic catalysts for gold nanorods etching: development of an ultrasensitive genosensor for detection of H. pylori. Sensor. Actuator. B. Chem.371, 132600 (2022).
   Web of Science ®Google Scholar
• Gopinath V , PriyadarshiniS , MubarakAliDet al. Anti-H. pylori, cytotoxicity and catalytic activity of biosynthesized gold nanoparticles: multifaceted application. Arab. J. Chem.12(1), 33–40 (2019).
   Web of Science ®Google Scholar
• Al-Radadi NS . Microwave assisted green synthesis of Fe@Au core–shell NPs magnetic to enhance olive oil efficiency on eradication of H. pylori [life preserver]. Arab. J. Chem.15(5), 103685 (2022).
   Web of Science ®Google Scholar
• El-Moaty HIA , SolimanNA , HamadRS , IsmailEH , SabryDY , KhalilMMH. Comparative therapeutic effects of Pituranthos tortuosus aqueous extract and phyto-synthesized gold nanoparticles on H. pylori, diabetic and cancer proliferation. South Afr. J. Botany139, 167–74 (2021).
   Web of Science ®Google Scholar
• Thamphiwatana S , GaoW , ObonyoM , ZhangL. In vivo treatment of H. pylori infection with liposomal linolenic acid reduces colonization and ameliorates inflammation. Proc. Natl Acad. Sci. USA111(49), 17600–5 (2014).
   PubMed Web of Science ®Google Scholar
• Obonyo M , ZhangL , ThamphiwatanaS , PornpattananangkulD , FuV , ZhangL. Antibacterial activities of liposomal linolenic acids against antibiotic-resistant H. pylori. Mol. Pharmaceut.9(9), 2677–85 (2012).
   PubMed Web of Science ®Google Scholar
• Jain P , JainS , PrasadKN , JainSK , VyasSP. Polyelectrolyte coated multilayered liposomes [nanocapsules] for the treatment of H. pylori Infection. Mol. Pharmaceut.6(2), 593–603 (2009).
   PubMed Web of Science ®Google Scholar
• Bardonnet P , FaivreV , BoullangerP , PiffarettiJ , FalsonF. Pre-formulation of liposomes against H. pylori: characterization and interaction with the bacteria. Eur. J. Pharmaceut. Biopharmaceut.69(3), 908–22 (2008).
   PubMed Web of Science ®Google Scholar
• Wu Y , GengJ , ChengXet al. Cosmetic-derived mannosylerythritol lipid-B-phospholipid nanoliposome: an acid-stabilized carrier for efficient gastromucosal delivery of amoxicillin for in vivo treatment of H. pylori. ACS Omega7(33), 29086–99 (2022).
   PubMed Web of Science ®Google Scholar
• Osborne N , CataniaR , Stolnik-TrenkicS , FalconeFH , RobinsonK. A liposomal drug delivery system for improved eradication of H. pylori. Access Microbiol.1(1A), (2019).
   Google Scholar
• Xing H , HwangK , LuY. Recent developments of liposomes as nanocarriers for theranostic applications. Theranostics6(9), 1336–52 (2016).
   PubMed Web of Science ®Google Scholar
• Lai Y , WeiW , DuY , GaoJ , LiZ. Biomaterials for H. pylori therapy: therapeutic potential and future perspectives. Gut Microbes14(1), 2120747 (2022).
   PubMed Web of Science ®Google Scholar
• Wang R , SongC , GaoAet al. Antibody-conjugated liposomes loaded with indocyanine green for oral targeted photoacoustic imaging-guided sonodynamic therapy of H. pylori infection. Acta Biomater.143, 418–27 (2022).
   PubMed Web of Science ®Google Scholar
• Deng G , WuY , SongZet al. Tea polyphenol liposomes overcome gastric mucus to treat H. pylori infection and enhance the intestinal microenvironment. ACS Appl. Mater. Interf.14(11), 13001–12 (2022).
   PubMed Web of Science ®Google Scholar
• Wang Y , WuS , WangLet al. The activity of liposomal linolenic acid against H. pylori in vitro and its impact on human fecal bacteria. Front. Infect. Microbiol.12:865320 (2022).
   PubMedGoogle Scholar
• Seabra CL , NunesC , Gomez-LazaroMet al. Docosahexaenoic acid loaded lipid nanoparticles with bactericidal activity against H. pylori. Int. J. Pharmaceut.519(1–2), 128–37 (2017).
   PubMed Web of Science ®Google Scholar
• Lopes-de-Campos D , PintoRM , LimaSACet al. Delivering amoxicillin at the infection site – a rational design through lipid nanoparticles. Int. J. Nanomed.14, 2781–95 (2019).
   PubMed Web of Science ®Google Scholar
• Sharaf M , ArifM , KhanSet al. Co-delivery of hesperidin and clarithromycin in a nanostructured lipid carrier for the eradication of H. pylori in vitro. Bioorgan. Chem.112, 104896 (2021).
   PubMed Web of Science ®Google Scholar
• Francis JE , SkakicI , DekiwadiaCet al. Solid lipid nanoparticle carrier platform containing synthetic TLR4 agonist mediates non-viral DNA vaccine delivery. Vaccines8(3), 551 (2020).
   Web of Science ®Google Scholar
• Yadav HKS , AlmokdadAA , shalufSIM , DebeMS. Polymer-based nanomaterials for drug-delivery carriers. In: Nanocarriers for Drug Delivery.Elsevier, UK, 531–56 (2019).
   Google Scholar
• Vrignaud S , BenoitJP , SaulnierP. Strategies for the nanoencapsulation of hydrophilic molecules in polymer-based nanoparticles. Biomaterials32(33), 8593–604 (2011).
   PubMed Web of Science ®Google Scholar
• Lin YH , LinJH , ChouSCet al. Berberine-loaded targeted nanoparticles as specific H. pylori eradication therapy: in vitro and in vivo study. Nanomedicine10(1), 57–71 (2015).
   PubMed Web of Science ®Google Scholar
• Harsha S . Dual drug delivery system for targeting H. pylori in the stomach: preparation and in vitro characterization of amoxicillin-loaded Carbopol® nanospheres. Int. J. Nanomed.7, 4787-4796 (2012).
   PubMed Web of Science ®Google Scholar
• Arif M , AhmadR , SharafMet al. Antibacterial and antibiofilm activity of mannose-modified chitosan/PMLA nanoparticles against multidrug-resistant H. pylori. Int. J. Biol. Macromol.23, 418–32 (2022).
   Google Scholar
• Li P , ChenX , ShenYet al. Mucus penetration enhanced lipid polymer nanoparticles improve the eradication rate of H. pylori biofilm. J. Control. Release300, 52–63 (2019).
   PubMed Web of Science ®Google Scholar
• Meng F , TaoH , MiYet al. Nanocluster-mediated photothermia improves eradication efficiency and antibiotic sensitivity of H. pylori. Cancer Nanotechnol.13(11), 13 (2022).
   Google Scholar
• Umamaheshwari RB , JainNK. Receptor mediated targeting of lectin conjugated gliadin nanoparticles in the treatment of H. pylori. J. Drug Target.11(7), 415–24 (2003).
   PubMed Web of Science ®Google Scholar
• Ramteke S , JainNK. Clarithromycin- and omeprazole-containing gliadin nanoparticles for the treatment of H. pylori. J. Drug Target.16(1), 65–72 (2008).
   PubMed Web of Science ®Google Scholar
• Gonçalves RFS , MartinsJT , DuarteCMM , VicenteAA , PinheiroAC. Advances in nutraceutical delivery systems: From formulation design for bioavailability enhancement to efficacy and safety evaluation. Trends Food Sci. Technol.78, 270–91 (2018).
   Web of Science ®Google Scholar
• Jaiswal M , DudheR , SharmaPK. Nanoemulsion: an advanced mode of drug delivery system. 3 Biotech.5(2), 123–7 (2015).
   PubMedGoogle Scholar
• Tran LTC , GueutinC , FrebourgG , BurucoaC , FaivreV. Erythromycin encapsulation in nanoemulsion-based delivery systems for treatment of H. pylori infection: protection and synergy. Biochem. Biophys. Res. Comm.493(1), 146–51 (2017).
   PubMed Web of Science ®Google Scholar
• Lin YH , ChiouSF , LaiCHet al. Formulation and evaluation of water-in-oil amoxicillin-loaded nanoemulsions using for H. pylori eradication. Process Biochem.47(10), 1469–78 (2012).
   Web of Science ®Google Scholar
• Yang Y , ChenL , SunH-Wet al. Epitope-loaded nanoemulsion delivery system with ability of extending antigen release elicits potent Th1 response for intranasal vaccine against H. pylori. J. Nanobiotechnol.17(1), 6 (2019).
   PubMed Web of Science ®Google Scholar
• Prasetya YA , NisyakK , AmandaER. Antibacterial Activity of Galangal (Alpinia galanga L. Willd) Oil Nanoemulsion inInhibiting the Growth of Helicobacter pylori. Biotropika: J. Tropical Biol.7(30), 136–42 (2019).
   Google Scholar
• Chen X , ZouY , ZhangSet al. Multi-functional vesicles improve H. pylori eradication by a comprehensive strategy based on complex pathological microenvironment. Acta Pharm. Sin. B.12(9), 3498–3512 (2022).
   PubMed Web of Science ®Google Scholar
• Wu T , WangL , GongMet al. Synergistic effects of nanoparticle heating and amoxicillin on H. pylori inhibition. J. Magn. Magn. Mater.485, 95–104 (2019).
   Web of Science ®Google Scholar
• Jing ZW , JiaYY , WanNet al. Design and evaluation of novel pH-sensitive ureido-conjugated chitosan/TPP nanoparticles targeted to H. pylori. Biomaterials84, 276–85 (2016).
   PubMed Web of Science ®Google Scholar
• Qaiser A , KianiMH , ParveenRet al. Design and synthesis of multifunctional polymeric micelles for targeted delivery in H. pylori infection. J. Mol. Liq.363, 119802 (2022).
   Web of Science ®Google Scholar
• Arif M , DongQJ , RajaMA , ZeenatS , ChiZ , LiuCG. Development of novel pH-sensitive thiolated chitosan/PMLA nanoparticles for amoxicillin delivery to treat H. pylori. Mater. Sci. Engin. C.83, 17–24 (2018).
   PubMed Web of Science ®Google Scholar
• Rosen BP . Transport and detoxification systems for transition metals, heavy metals and metalloids in eukaryotic and prokaryotic microbes. Comparat. Biochem. Physiol. A: Mol. Integrat. Physiol.133(3), 689–93 (2002).
   PubMed Web of Science ®Google Scholar
• Felice B , PrabhakaranMP , RodríguezAP , RamakrishnaS. Drug delivery vehicles on a nano-engineering perspective. Mater. Sci. Engin.: C.41, 178–95 (2014).
   PubMed Web of Science ®Google Scholar
• Panáček A , KvítekL , SmékalováMet al. Bacterial resistance to silver nanoparticles and how to overcome it. Nature Nanotechnol.13(1), 65–71 (2018).
   PubMed Web of Science ®Google Scholar
• Cardos IA , ZahaDC , SindhuRK , CavaluS. Revisiting therapeutic strategies for H. pylori treatment in the context of antibiotic resistance: focus on alternative and complementary therapies. Molecules26(19), 6078 (2021).
   PubMed Web of Science ®Google Scholar
• Sosnik A , AugustineR. Challenges in oral drug delivery of antiretrovirals and the innovative strategies to overcome them. Adv. Drug Deliv. Rev.103, 105–20 (2016).
   PubMed Web of Science ®Google Scholar
• Plaza-Oliver M , Santander-OrtegaMJ , LozanoMV. Current approaches in lipid-based nanocarriers for oral drug delivery. Drug Deliv. Translat. Res.11(2), 471–97 (2021).
   PubMed Web of Science ®Google Scholar
• Spirescu VA , ChircovC , GrumezescuAM , AndronescuE. Polymeric nanoparticles for antimicrobial therapies: an up-to-date overview. Polymers.13(5), 724 (2021).
   PubMed Web of Science ®Google Scholar
• Huwyler J , KettigerH , SchipanskiA , WickP. Engineered nanomaterial uptake and tissue distribution: from cell to organism. Int. J. Nanomed.8, 3255–3269 (2013).
   PubMed Web of Science ®Google Scholar
• Wu LP , WangD , LiZ. Grand challenges in nanomedicine. Mater. Sci. Engin.: C.106, 110302 (2020).
   PubMed Web of Science ®Google Scholar
• Vital JS , TanoeiroL , Lopes-OliveiraR , ValeFF. Biomarker characterization and prediction of virulence and antibiotic resistance from H. pylori next generation sequencing data. Biomolecules12(5), 691 (2022).
   PubMed Web of Science ®Google Scholar
• Zhu X , SuT , WangS , ZhouH , ShiW. New advances in nano-drug delivery systems: H. pylori and gastric cancer. Front.Oncol.12, 834934 (2022).
   PubMed Web of Science ®Google Scholar
• Safarov T , KiranB , BagirovaM , AllahverdiyevAM , AbamorES. An overview of nanotechnology-based treatment approaches against H. pylori. Expert Rev. Anti-Infect. Ther.17(10), 829–40 (2019).
   PubMed Web of Science ®Google Scholar
• Aflakian F , MirzaviF , AiyelabeganHTet al. Nanoparticles-based therapeutics for the management of bacterial infections: a special emphasis on FDA approved products and clinical trials. Eur. J. Pharmaceut. Sci.188, 106515 (2023).
   PubMed Web of Science ®Google Scholar
• Zazo H , ColinoCI , LanaoJM. Current applications of nanoparticles in infectious diseases. J. Control. Release224, 86–102 (2016).
   PubMed Web of Science ®Google Scholar